|PINHEIRO, PATRICIA - Cornell University - New York|
|BEREMAN, MICHAEL - North Carolina State University|
|BURD, JOHN - Retired ARS Employee|
|Armstrong, John - Scott|
|Thannhauser, Theodore - Ted|
|MACCOSS, MICHAEL - University Of Washington|
Submitted to: Journal of Proteome Research
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/5/2014
Publication Date: 3/31/2014
Citation: Pinheiro, P., Bereman, M., Burd, J., Pals, M.A., Armstrong, J.S., Howe, K.J., Thannhauser, T.W., Maccoss, M., Gray, S.M., Cilia, M. 2014. Evidence for the biochemical basis of host virulence in the greenbug aphid, Schizaphis graminum (Homoptera: Aphididae). Journal of Proteome Research. 13(4):2094–2108.
Interpretive Summary: Insects damage plants when they feed on them. They also transmit pathogens that cause disease and crop loss. Some crops do not succumb to feeding by insects while other crops do. This variation depends on the plant’s genetic make-up and also the insect’s genetic make-up. Wheat and other small grain crops are especially at risk to feeding by the greenbug, a tiny insect that uses its needle-like mouthparts to suck the juice from within the plant’s vascular system. Insecticides and cereal varieties that are resistant to insect feeding are widely used to control greenbug infestation. Plants also produce compounds, called defense compounds, to help defend them against herbivory by insects. Occasionally though, greenbug populations emerge that are especially damaging, or virulent, to wheat and can’t be easily controlled by these methods. In this study, we show that virulent greenbugs are able to damage so many wheat varieties because they express molecules, called proteins, which help them cope with plant defense compounds better than other greenbugs. They also reproduce better than other greenbugs, which may give them an advantage in the field compared to other greenbugs. We also show that the generation of new virulent greenbugs happens when the insects reproduce sexually. This result is important because now we better understand that new virulent greenbugs don’t emerge as a consequence of planting greenbug-resistant wheat varieties. The finding also has implications for our understanding of future outbreaks of greenbugs due to changing climate conditions and overwintering habits of the insect where the insects will be able to reproduce sexually in new geographic areas.
Technical Abstract: Biotypes of aphids and many other insect pests are defined based on the phenotypic response of host plants to the insect pest without considering their intrinsic characteristics and genotypes. Plant breeders have spent considerable effort to develop aphid-resistant, small grain varieties to limit insecticide control of the greenbug, Schizaphis graminum. However, new S. graminum biotypes frequently emerge that break resistance. Mechanisms of virulence on the aphid side of the plant-insect interaction are not well understood. S. graminum biotype H is highly virulent on most small grain varieties. This characteristic makes biotype H ideal for comparative proteomics to investigate the basis of biotype virulence in aphids. In this study, we used comparative proteomics to identify protein expression differences associated with virulence. Aphid proteins involved in the tricarboxylic acid cycle, immune system, cell division, and anti-apoptosis pathways were found to be up-regulated in biotype H relative to other biotypes. Proteins from the bacterial endosymbiont of aphids were also differentially expressed in biotype H. Guided by the proteome results, we tested whether biotype H had a fitness advantage compared to other S. graminum biotypes and found that biotype H had a higher reproductive fitness as compared to two other biotypes on a range of different wheat germplasms. Finally, we tested whether aphid genetics can be used to further dissect the genetic mechanisms of biotype virulence in aphids. The genetic data showed that sexual reproduction is a source of biotypic variation observed in S. graminum.